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The potential of intramammary administered cephapirin and cephalonium to select for ESBL-producing E. coli in the bovine gut and in dairy manure
Speksnijder, D.; Kusters, N.;...
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Objectives: Selection and spread of Extended Spectrum Beta-lactamase (ESBL)-producing Enterobacteriaceae within animal production systems and potential spill over to humans is a major concern. Orally applied cephalosporins can select for antimicrobial resistant organisms in the gastrointestinal tract. There is however limited research on the effect of non- oral, locally applied, antimicrobials on the selection of resistant organisms in the gastrointestinal tract. First generation cephalosporins are widely used to treat and prevent intramammary infections in dairy cows. We studied the potential effects of low doses of cephapirin (CP) and cephalonium (CL) to select for ESBL producing E. coli in fresh faecal fermentations and in the manure of adult dairy cows as a model for intramammary application of cephapirin, because the minimal concentration which still selects for resistance (MSC) is unknown in a complex environment like the gastrointestinal tract.
Materials and Methods: A literature search has been conducted, to determine the test conditions for the MSC testing and to predict the maximum expected concentrations of CP in the intestinal content and in the manure of dairy cows after intramammary treatment.
Three different laboratory experiments have been conduct- ed on samples from The Netherlands, Germany, Belgium and the United Kingdom.
1): Competition assay in rich culture media at 370C. From every country, 3 ESBL and 3 non-ESBL E. coli isolates from dairy farms have been collected. A 1:3 ratio mixture of these ESBL and non-ESBL isolates under nine different conditions have been tested for their potential to select for Cefotaxime (CTX) resistance as an indicator for ESBL selection: no antibiotics baseline; no antibiotics (blank condition); 0.25 μg/ml CTX; 0.04, 0.4 and 4.0 μg/ml of CL; 0.08, 0.8 and 8.0 μg/ml of CP. After 6 h of incubation the percentage of resistant colo- nies to CTX in each of the different test conditions have been assessed to determine the MSC of CP and CL for ESBL pro- ducing E. coli.
2): Competition assay in fecal fermentations at 370C. Freshly derived manure samples from 10 different healthy dairy cows were pooled and were spiked with the 3 ESBL and 3 non-ESBL E. coli isolates at 107 CFU/ml in 9 different tubes containing anaerobic standard ileal efflux medium. A comparable approach as in experiment 1 has been followed to determine the MSCs for ESBL producing E. coli in freshly derived fecal fermentations of dairy cows.
3): Competition assay in dairy manure. Manure pit samples from each country where taken. The same procedures were being followed as in experiment 2, however at a temperature of 170C.
Results: In experiment 1, a significant (p=0.007) increase in CTX resistant colonies was seen between a 0.8 μg/ml (45% resistant) and a 8.0 μg/ml (96% resistant) concentration of CP. No significant increase from 0.08 (38%) to 0.8 μg/ml was ob- served. A significant (p=0.023) increase in CTX resistant colonies was seen between a 0.4 μg/ml (41% resistant) and a 4.0 μg/ml (90% resistant) concentration of cephalonium.
In experiment 2, a borderline significant (p=0.079) increase in CTX resistant colonies was seen between a 0.8 μg/ml (44% resistant) and a 8.0 μg/ml (75% resistant) concentration of CP. The results were skewed by the unexpectedly low number of CTX resistant colonies from the Belgian samples. In the experiment with different concentrations of CL (0.04, 0.4 and 4.0 μg/ ml), no significant differences in CTX resistant colonies was observed (respectively 78%, 88% and 91%).
In experiment 3, no increases in CTX resistant colonies have been observed in the CP and CL group at each of the tested concentrations.
Based on available literature on pharmacodynamics and pharmacokinetics of CP and CL in dairy cows, the maximum expected concentration of CP and CL in the intestinal content of adult dairy cows after intramammary treatment according to the label will most probably not exceed 0.29 μg/ml. The expected maximum concentration of CP and CL in manure pits of average dairy farms will not exceed 0.03 μg/ml.
Conclusions: We found that the expected concentrations of cephapirin in the gut and manure pits are at least 10 fold lower than the MSC of cephapirin to select for CTX resistance in the different environments. Thus, the potential of intramammary administered cephapirin to select for ESBL-producing E. coli in the bovine gut and in manure pits seems low.
Keywords: Antimicrobial resistance, intramammary, cep- hapirin, cephalonium, dairy cow.
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About
Affiliation of the authors at the time of publication
Faculty of Veterinary Medicine, Utrecht University, Utrecht, Netherlands;
MSD Animal Health, Boxmeer, Netherlands;
Department of Veterinary and Animal Sciences, University of Copenhagen, Copenhagen, Denmark;
Quality Milk Management Services Ltd, Easton, United Kingdom;
Animal Health Care Flanders, Torhout, Belgium.
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